Mar Biodiv (2012) 42:65–72 DOI 10.1007/s12526-011-0093-0

ORIGINAL PAPER

Differential morphological features of two Dendronephthya soft coral species suggest differences in feeding niches

Michal Grossowicz & Yehuda Benayahu

Received: 23 February 2011 /Revised: 31 March 2011 /Accepted: 1 April 2011 /Published online: 3 May 2011 # Senckenberg, Gesellschaft für Naturforschung and Springer 2011

Abstract Octocorals are characterized by pinnate tentacles Keywords Octocorallia . Polyp morphology. Gause’s and internal sclerites. Their feeding ability is determined by Law. Sclerites . Niche overlap . Feeding . Red Sea the morphological features of the polyps. Capture of their food by these corals is also affected by the flexibility of the colony, which in turn is determined by the features of the Introduction sclerites. We studied the morphological features of two azooxanthellate octocorals, Dendronephthya hemprichi and The sub-class Octocorallia (Cnidaria: Anthozoa) comprises D. sinaiensis, whose depth distribution partially overlaps at more than 2,000 species, with a worldwide distribution and Eilat (northern Red Sea). Following Gause’s Law, such found in a variety of habitats (Bayer 1973; Fabricius and coexistence is considered to be possible if each species is Alderslade 2001). Octocorals are characterized by polyps adapted to utilize different food items. In order to examine with eight pinnate tentacles and internal calcareous skeletal this Law, the features of the polyps of the two species and elements, termed sclerites. The octocoral order Alcyonacea their sclerites were studied. Each side of their tentacles is the largest and the member species may or may not displays 11–13 pinnules, which are longer at the tentacles’ contain symbiotic algae in their tissue (they are zooxanthellate distal end compared to its median section and proximal end, vs. azooxanthellate species, respectively). Alcyonacean spe- with the distal pinnules of D. sinaiensis being longer than cies constitute the second most important benthic component those of D. hemprichi. At the proximal end of the tentacles on many coral reefs, including those of the Gulf of Aqaba of D. sinaiensis, the pinnules emerge perpendicularly, (northern Red Sea) (Benayahu and Loya 1977, 1981). unlike in D. hemprichi, where they emerge from the lateral Goldberg (1973) and Kinzie (1973) reported that various sides; the distance between the rows of pinnules is, gorgonian octocoral species are adapted to specific depths therefore, shorter for the former. These findings imply that that are related to the prevailing current regime. Depth the filtered phytoplankton by the two species may differ in partitioning between congeneric octocorals was described size. Their sclerites also differ in size and shape, and for Plexaura homomalla and P. nina in the US Virgin therefore the expansion and contraction abilities of their Islands, with a 20 m limit of occurrence for the former and polyps also differ, and may thus affect their respective >20 m for the latter (Lasker et al. 1983). The size of the feeding abilities. The findings indicate that D. hemprichi polyps of these two species was found to be related to their and D. sinaiensis are adapted to utilize different food items, feeding rates, i.e., the larger polyps of P. nina exhibit a and therefore support Gause’s Law and explain the higher feeding rate than the smaller ones of P. homomalla. coexistence of the two species. Heterotrophy and photoautotrophy, however, were not the only factors that explained the depth partitioning of these : M. Grossowicz Y. Benayahu (*) species. Department of Zoology, George S. Wise Faculty of Life Sciences, The feeding rate of an octocoral colony is determined by Tel Aviv University, the morphological features of its tentacles, including the Ramat Aviv, Tel Aviv 69978, Israel length of the pinnules, their shape and density, as well as by e-mail: [email protected] the ambient flow speed (Sebens and Johnson 1991). 66 Mar Biodiv (2012) 42:65–72

Among octocorals, the narrowly-spaced pinnules are examined whether the two species possess polyps with arranged in a typical comb-like structure along each of the different morphological features. Such differences may in tentacle margins, making them suitable for filter feeding on turn lead to differential feeding capabilities that reduce small particles (Fabricius and Alderslade 2001). The polyps competition for food, following Gause’s(1934) Law that feed most effectively under an optimum ambient velocity, two similar species dwelling in the same habitat displace which determines their feeding performance and food each other in such a manner that each takes position of niche, which are also related to the morphological features certain peculiar kind of food. Food, such as phytoplankton, of the polyps (Dai and Lin 1993). Capture of food particle is a limited resource in the oligotrophic and phytoplankton by the polyps is also determined by their sclerites low value Red Sea (Lindell and Post 1995), especially composition and arrangement (Vogel 1981). While some during the summer period, when the water is nutrient- types of sclerites may limit the expansion of the octocoral depleted (Reiss and Hottinger 1984). colonies, including their polyps, others may limit their contraction (Lewis and von Wallis 1991). Notably, there is an intraspecific variation in the morphological features of Materials and methods octocoral polyps that is related to their feeding capabilities and exploitation of the available food items (Kinzie 1973; The study was conducted at the EAPC oil jetties, located Sponaugle and LaBarbera 1991; Lin and Dai 1996). 4 km south of the city of Eilat (Fig. 1), constructed in the The azooxanthellate alcyonaceans of the genus Dendro- late 1960s and considered as an unplanned artificial reef nephthya (family Nephtheidae) are common in the northern (Dahan and Benayahu 1997a, b; Perkol-Finkel and Red Sea where they inhabit steep reef slopes (Benayahu Benayahu 2004). Identification of colonies of D. hempri- 1985; Dahan and Benayahu 1997b). D. hemprichi has a chi Klunzinger, 1877 and D. sinaiensis Verseveldt, 1970 wide Indo-Pacific distribution (Verseveldt 1965) while D. was facilitated by comparison with their respective type sinaiensis has been found so far only in the northern Red material kept at the Berlin Museum für Naturkunde and Sea (Verseveldt 1970). The taxonomy of the genus the Zoological Museum of Tel Aviv University. In order to Dendronephthya is quite problematic and there are no compare between the morphological features of the polyps efficient tools to determine species adequately, nor is there of the two species, branches, ca 10 cm in length (n=8–10 any known phylogenetic molecular signal (McFadden et al. for each species), were removed from different colonies 2010). When alive, however, D. hemprichi and D. growing on the jetty-pillars at depths of 10 and 22 m, sinaiensis are distinguishable from one another on Eilat respectively (April–May2007).Thesetwodepthsrepre- reefs, and taxonomic identification of preserved colonies sent the highest colony density of the two species can be properly conducted by comparing them to their (Grossowicz 2008). The branches were brought to the respective types (see below). Both species successfully Interuniversity Institute of Marine Sciences at Eilat (IUI) flourish on various underwater artificial structures (Perkol- andplacedinflow-throughseawatertanks.Adaylater,the Finkel and Benayahu 2004, 2005). In Eilat (northern tip of branches were transferred into 500 ml plastic containers the Gulf of Aqaba, Red Sea), they colonize the vertical steel filled with aerated seawater and, when fully inflated, they pillars of Eilat's oil jetties (Eilat-Ashqelon Pipe Line Company; EAPC), which are characterized by a high-flow regime (Perkol-Finkel and Benayahu 2004). D. hemprichi and D. sinaiensis display a partially overlapping depth distribution along the pillars. The former is found at 1–32 m and the latter at 11–32 m (Grossowicz 2008). The two species are passive phytoplankton filter feeders, and were the first ever recorded feeding on these food items among members of the class Anthozoa (Fabricius et al. 1995a, b). Their life history traits exhibit similarity: both are gonochoric broad- casters (Barki 1992; Dahan and Benayahu 1997a, 1998)and feature asexual propagation by means of numerous small autonomous fragments (Barki 1992; Dahan and Benayahu 1997b). The above-noted traits of D. hemprichi and D. sinaiensis thus reveal a remarkable degree of biological and ecological similarity. D. Fig. 1 Study site at Eilat, northern tip of the Gulf of Aqaba (Red Sea) Intrigued by the distributional pattern along depth of (EAPC Eilat-Ashqelon Pipe Line Company, IUI The Interuniversity hemprichi and D. sinaiensis (see above), this study Institute for Marine Sciences) Mar Biodiv (2012) 42:65–72 67

10% sodium hypochloride, air-dried and gold-coated. The polyps and the sclerites were examined under a JEOL JSM 840a scanning electron microscope (SEM). The SEM micrographs were used to determine the following mor- phometric features of the polyps of each species: length of tentacles, number of pinnules along a tentacle margin, length of pinnules, and distance between rows of pinnules on a given tentacle. For each of the species, the first 1–4 pinnules along each margin of the tentacle were classed as proximal, the following 5–8 pinnules as median, and the remainder (up to 12–13) as distal. The length and width of the different types of sclerites found in the polyps were measured using an Olympus Soft Imaging System (SIS) Scandium to the nearest 0.01 mm Fig. 2 Tentacles: a Dendronephthya hemprichi, b D. sinaiensis (51 sclerites of each species). The length-to-width ratio of the spindles was calculated for each species. Addi- were relaxed by the introduction of magnesium sulfate tionally, in order to characterize the arrangement of the (10%) (see Vasconcelos et al. 2006). After relaxation took sclerites in the polyp, polyps from three different place, 12–16 polyps from each branch were clipped off by colonies of both species were removed, subjected to scissors and preserved in 2.5% seawater glutaraldehyde. dehydration in xylene overnight, and examined under a These polyps were used for determination of their light microscope (Nikon DS-Fi1). morphological features following decalcification. The All statistical analyses were performed by Statistica 7.1. polyps were decalcified in a mixture of equal volumes of Average values were compared by Student’s t test for formic acid (50%) in sodium citrate (15%) for 30 min and independent samples. Variance was tested by F test and then replaced in 2.5% glutaraldehyde (Yacobovitch et al. homogeneity of data was tested by Cochran C. one-way 2003). The polyps underwent dehydration through a ANOVA followed by Bonferroni post-hoc. Normality of the graded series of ethanol (from 30 to 99%), critically dependant variables was assessed by the Kolmogorov– point-dried with liquid CO2 and then gold-coated. Scler- Smirnov test (KS). All values are presented at a confidence ites were isolated from several other polyps (ca 10) using interval of 95%.

Fig. 3 Scanning electron micrographs: a, b tentacles of Dendronephthya hemprichi, c, d tentacles of D. sinaiensis 68 Mar Biodiv (2012) 42:65–72

Table 1 Dendronephthya hemprichi and D. sinaiensis: comparison between average length of proximal, median and distal pinnules along the tentacle, and average distance between rows of adjacent pinnules (mm ± SD)

Morphological features Proximal pinnules Median pinnules Distal pinnules Statistics (1–4) (5–8) (9-12/13)

D. hemprichi Average length of pinnules 0.080±0.030 (n=67)* 0.160±0.38 (n=72) 0.149±0.49 (n=46) One-way ANOVA p=0 Average distance between rows of pinnules 0.050±0.008 (n=19) – 0.056±0.007 (n=19) t test p=0.02* D. sinaiensis Average length of pinnules 0.091±0.038 (n=40)* 0.174±0.049 (n=52) 0.192±0.043 (n=35) One-way ANOVA p=0 Average distance between rows of pinnules 0.028±0.005 (n=10) – 0.052±0.005 (n=11) t test p=0*

– No data, n sample size, *significant difference

Results between the morphological features of the two species did not reveal significant differences (Table 2). In addition, the Each side of the eight tentacles of D. hemprichi and of D. distance between two adjacent pinnules was measured for sinaiensis features one row of 11–13 pinnules (n=20 bothspeciesasanindication of pinnules density: D. hemprichi: tentacles examined for D. hemprichi and n=17 for D. 0.024±0.018 mm, n =6 vs. D. sinaiensis: 0.0184±0.007 mm, sinaiensis). In D. hemprichi, the pinnules emerge from the n=9, and did not significantly differ (p=0.11). lateral sides along the entire length of the tentacle and are Polyps of both D. hemprichi and D. sinaiensis contain mostly directed outwards (Figs. 2a and 3a, b). In D. spindles up to 3 and 2.5 mm respectively (Fig. 4a, b), which sinaiensis, at the proximal end of the tentacle the pinnules comprise the supporting bundle (see Fabricius and Alderslade emerge perpendicularly from its upper (oral) surface 2001). The polyp head features shorter spindles up to 0.5 mm (Figs. 2b and 3c, d). (Fig. 4c, d, respectively). Both types of sclerites are covered Comparisons between the length of the proximal and distal with rather evenly scattered warts. The tentacle sclerites are pinnules (Fig. 2) and the distance between their rows in D. from 0.02 to 0.1 mm long (Fig. 4e, f, respectively). In hemprichi and D. sinaiensis are presented in Table 1 (data addition, the stalk of D. sinaiensis features short and thick were normally distributed, KS, p>0.1). In both species, the antler-shaped sclerites (Bayer et al. 1983), up to 0.1 mm proximal pinnules (1–4) were significantly shorter than the (Fig. 5), which are not found in D. hemprichi. The average median and distal ones (5–8 and 9-12/13). In both D. length-to-width ratio of the spindles of D. hemprichi is hemprichi and D. sinaiensis the distance between the rows 11.71±3.04, and D. sinaiensis is 17.53±5.73 (n=51 sclerites of the proximal pinnules was significantly shorter than that examined for each species), with a significantly lower ratio between the distal ones (t test, p=0.02, p=0, respectively). for the former compared to the latter [all ratios normally Table 2 presents a comparison between the morphological distributed (KS, p>0.02) with a non-similar variance (F-test, features of the two species, revealing that D. hemprichi has p<0.05), t-test p<0.001], making the D. sinaiensis spindle- longer tentacles than D. sinaiensis.InD. sinaienis,thedistal shaped sclerites much narrower. In both species, the spindles pinnules are significantly longer than those of D. hemprichi, are arranged in the characteristic polyp armature known for and the distance between the two rows at the proximal end is the genus Dendronephthya (Fabricius and Alderslade 2001). shorter than in D. hemprichi (p<0.01 for both, data were Light microscopy examination did not reveal any striking normally distributed, KS, p>0.1). All other comparisons difference in sclerite arrangement in the two species.

Table 2 Dendronephthya hemprichi and D. sinaiensis: comparison between average morphological features of polyps (mm ± SD)

Morphological features D. hemprichi D. sinaiensis t test n n p Average length of tentacle 0.667±0.108 ( =19) 0.560±0.109 ( =13) =0.01* Number of pinnules along margin of tentacle 11–13 ( n=20) 11–13 ( n=17) Average length of proximal pinnules (1–4) 0.080±0.030 ( n=67) 0.091±0.038 ( n=40) p=0.09 Average length of median pinnules (5–8) 0.160±0.38 ( n=72) 0.174±0.049 ( n=52) p=0.08 Average length of distal pinnules (9–12/13) 0.149±0.49 ( n=46) 0.192±0.043 ( n=35) p=0* Average distance between adjacent rows of proximal pinnules 0.050±0.008 ( n=19) 0.028±0.005 ( n=10) p<<0.05* Average distance between adjacent rows of distal pinnules 0.056±0.007 ( n=19) 0.052±0.005 ( n=11) p=0.15 n Sample size, *significant difference Mar Biodiv (2012) 42:65–72 69

Fig. 4 Scanning electron micrographs of sclerites; spindles of supporting bundle: a D. hemprichi, b D. sinaiensis; spindles of polyp head: c D. hemprichi, d D. sinaiensis; tentacle sclerites: e D. hemprichi, f D. sinaiensis

Discussion such as a sieving mechanism (see Rubenstein and Koehl 1977). A filter feeder is most effective at collecting particles Filter feeding by marine organisms consists in the separa- only within a certain range of ambient water velocity and tion of particles from fluids by the use of porous media, particle sizes (Jørgensen 1955; Rubenstein and Koehl 1977; 70 Mar Biodiv (2012) 42:65–72

Fig. 5 Scanning electron micrographs of D. sinaiensis antlers

Vogel 1981). The comb-like pinnules along the margins of then Gause's (1934) Law is validated. Lasker et al. (1983), the tentacles of the genus Dendronephthya appear to be who examined the feeding rates of Plexaura homomalla more suitable for feeding on small particles or uptake of and P. nina (see also “Introduction”), concluded that the dissolved organic matter (DOM) than for capturing zoo- morphological differences between their polyps led to plankton (Fabricius et al. 1995a, b). Notably, the latter different feeding habits and feeding rates. It was assumed studies provided the first recorded evidence for feeding on that P. nina, which has larger polyps, is found at greater phytoplankton in Dendronephthya species. The density of depths with prevailing weaker currents compared to the pinnules indicates their suitability for filtering a certain shallower depths (Lasker et al. 1983, Witman and Dayton particle size (Rubenstein and Koehl 1977). The denser the 2001). Since in our study a significant difference was found pinnules, the greater their chance of capturing small between the length of the tentacles of the polyps of D. particles; while the more they are elongated, the greater hemprichi and D. sinaiensis, the difference between the the surface area for such capture, and thus capture particle sizes that they consume can be related to both the efficiency (Lasker et al. 1983). The length of the pinnules length of the pinnules and the distance between rows of at the distal end of a D. sinaiensis tentacle is significantly pinnules along the tentacle as well as to the tentacles length. greater than in D. hemprichi (Table 2). The filtering abilities These results supply a solid background for future and, consequently, the size of the food particles ingested by experimental work aimed at verifying the above. the two species are thus expected to differ. In D. sinaiensis, Both D. hemprichi and D. sinaiensis posses the spindle- the distance between the two rows of pinnules at the shaped sclerites (Fig. 4a, b) that are characteristic of the proximal end of the tentacle is significantly smaller than in genus (Fabricius and Alderslade 2001). The antler-shaped D. hemprichi (0.028±0.005 vs. 0.050±0.008 mm respec- sclerites found in D. sinaiensis are smaller compared to the tively, Table 2, p<<0.05). Similarly, at D. sinaiensis, the spindles (0.1 vs. >1 mm: see Figs. 4b, d and 5). Indeed, it distance between rows at the proximal end of the tentacle is has been argued that Dendronephthya species displaying significantly smaller than between rows at its distal end antler-shaped sclerites should probably be assigned to (Table 1). Such a narrow space between the two rows of another genus (van Ofwegen, personal communication), pinnules at the proximal end of the tentacle is suggested to an issue that requires future studies. Since antlers are also assist transportation of the smaller filtered particles to the found in the tissue that surrounds the internal canals of the mouth-opening. For example, we assume that phytoplank- colony stalk (Fabricius and Alderslade 2001), it is unlikely ton particles in a size-range of 0.025–0.050 mm, such as the that they play any role in supporting the polyps or in the Red Sea dinoflagellates Ceratium fusus (see Post et al. feeding process. The spindle-shaped sclerites of D. sinaien- 2002) and Ceratocorys sp. (see Rutman and Fishelson sis are narrower than those of D. hemprichi (length-to- 1969) which are 0.025 and 0.050 mm in size, respectively width ratio 17.53±5.73 vs. 11.71±3.04, respectively; (Menden-Deuer et al. 2001), will be consumed by D. Fig. 4a, b), and the shape of the former might confer on hemprichi and not by D. sinaiensis. However, smaller the tentacles a certain flexibility (Lewis and von Wallis phytoplankton items, such as the green algae Nannochlor- 1991), thereby differentiating the filtering ability of the two opsis sp. and Tetraselmis sp. (Fabricius et al. 1995a, b) may studied species. The different flexibility of the tentacles of be captured easily by D. sinaiensis' longer and denser these two species is therefore also suggested to affect their pinnules (see “Results”). We also suggest that D. sinaiensis filtering ability. has a somewhat narrower feeding niche in contrast to D. Our findings have revealed significant differences in hemprichi, which seems to be a more generalist feeder. morphological features of the polyps of D. hemprichi and Therefore, if such a feeding-related partitioning of food D. sinaiensis, which may have led to differences in the size items does indeed exist in D. hemprichi and D. sinaiensis, of the phytoplankton items upon which they feed. Although Mar Biodiv (2012) 42:65–72 71 a long time has elapsed since Gause's (1934) Law was Dahan M, Benayahu Y (1997b) Clonal propagation by the azoox- Dendronephthya hemprichi proposed, it is still being cited (e.g., Wang et al. 2005; anthellate octocoral . Coral Reefs 16:5–12 Brucet et al. 2006; Gravel et al. 2006; Roney et al. 2009), Dahan M, Benayahu Y (1998) Embryogenesis, planulae longetivity, and its validity is still being tested (e.g., Mikami et al. 2004; and competence in octocoral Dendronephthya hemprichi. Inver- Roney et al. 2009). tebr Biol 117:271–280 Dai CF, Lin MC (1993) The effect of flow on feeding of three Our current morphological findings imply the likelihood – ’ gorgonians from southern Taiwan. J Exp Mar Biol Ecol 173:57 of agreement with Gause s principle, which can explain the 69 partial depth overlap of the two octocoral species, whose Fabricius KE, Benayahu Y, Genin A (1995a) Herbivory in asymbiotic coexistence is possible due to their different nutritional soft corals. Science 268:90–92 requirements in regard to a limited resource in an Fabricius KE, Genin A, Benayahu Y (1995b) Flow-dependent herbivory and growth in zooxanthellae-free soft corals. Limnol oligotrophic sea (Lindell and Post 1995). Future research Oceanogr 40:1290–1301 is still required, however, in order to determine the specific Fabricius K, Alderslade P (2001) Soft corals and sea fans: a preferences in terms of captured food items and feeding comprehensive guide to the tropical shallow water genera of the behavior of the studied species. central-west Pacific, the Indian Ocean and the Red Sea. Australian Institute of Marine Science and the Museum and Art Gallery of the Northern Territory Acknowledgments We thank the Interuniversity Institute for Marine Gause GF (1934) The struggle for existence. Williams and Wilkins, Sciences at Eilat (IUI) for the use of facilities and assistance. We thank Baltimore the Eilat-Ashqelon Pipe Line Company (EAPC) for cooperation and Goldberg W (1973) The ecology of the coral-octocoral communities the Israel Nature and National Parks Protection Authority for issuing off the southeast Florida coast: geomorphology, species compo- the collection permit. We acknowledge Y. Delaria for SEM work, A. sition and zonation. Bull Mar Sci 24:465–488 Shlagman for curatorial help, N. Paz for editorial assistance, and V. Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling Wexsler for graphic work. We thank C. Lueter, Museum fuer niche and neutrality: the continuum hypothesis. Ecol Lett 9:399– Naturkunde, Berlin, for placing type material at our disposal. The 409 study was in part supported by the Israel Cohen Chair in Environmental Grossowicz M (2008) Niche partitioning among three azooxanthellate Zoology (Y. B.) and a grant from The Porter School of Environmental soft coral species in Eilat (northern Red Sea). MSc Thesis, Tel-Aviv Studies (PSES) at Tel Aviv University. The article constitutes part of on University, Israel (in Hebrew with English summary) MSc thesis in Ecology and Environmental Quality at Tel-Aviv University Jørgensen CB (1955) Quantitative aspects of filter feeding in submitted by M. Grossowicz. invertebrate. Biol Rev 30:391–453 Kinzie RAIII (1973) The zonation of West Indian Gorgonians. Bull Mar Sci 23:93–155 Lasker HR, Gottfried MD, Coffroth MA (1983) Effects of depth on References feeding capabilities of two octocorals. Mar Biol 73:73–78 Lewis JC, von Wallis E (1991) The function of surface sclerites in gorgonians (Coelenterata, Octocorallia). Biol Bull 181:275– Barki Y (1992) Population ecology and genetic characteristics of the 288 soft coral Dendronephthya in the northern Gulf of Eilat, Red Sea. Lin MC, Dai CF (1996) Drag, morphology and mechanical properties MSc Thesis, Tel-Aviv University, Israel (in Hebrew with English of three species of octocorals. J Exp Mar Biol Ecol 201:13–22 summary) Lindell D, Post AF (1995) Ultraphytoplankton succession is triggered Bayer FM (1973) Colonial organization in octocorals. In: Brodman by deep winter mixing in the Gulf of Aqaba (Eilat), Red sea. RS, Cheetman AH, Oliver WA Jr (eds) Animal colonies Limnol Oceanogr 40:1130–1141 development and function through time. Dowden, Hutchinson McFadden SC, Sánchez JA, France SC (2010) Molecular phyloge- and Ross,Pennsylvenia, pp 69–93 netic insights into the evolution of Octocorallia: a review. Integr Bayer FM, Grasshoff M, Verseveldt J (1983) Illustrated trilingual Comp Biol 50:389–410 glossary of morphological and anatomical terms applied to Menden-Deuer S, Lessard EJ, Satterberg J (2001) Effect of preserva- Octocorallia. Brill, Leiden tion on dinoflagellate and diatom cell volume and consequences Benayahu Y (1985) Faunistic composition and patterns in the for carbon biomass predictions. Mar Ecol Prog Ser 222:41–50 distribution of soft corals (Octocorallia, Alcyonacea) along the Mikami OK, Kohda M, Kawata M (2004) A new hypothesis for coral reefs of Sinai peninsula. Proceedings of the 5th Interna- species coexistence: male–male repulsion promotes coexistence tional Coral Reefs Congress Tahiti 6:255–260 of competing species. Popul Ecol 46:213–217 Benayahu Y, Loya Y (1977) Space partitioning by stony corals soft Perkol-Finkel S, Benayahu Y (2004) Community structure of stony corals and benthic algae on coral reefs of northern Gulf of Eilat and soft corals on vertical unplanned artificial reefs in Eilat (Red-Sea). Helgol wiss Meeresunters 30:362–382 (Red Sea): comparison to natural reefs. Coral Reefs 23:195– Benayahu Y, Loya Y (1981) Competition for space among coral- 205 reef sessile organisms at Eilat, Red-Sea. Bull Mar Sci 31:514– Perkol-Finkel S, Benayahu Y (2005) Recruitment of benthic organ- 522 isms onto a planed artificial reef: shift in community structure Brucet S, Boix D, López-Flores R, Badosa A, Quintana XD (2006) one decade post-deployment. Mar Environ Res 59:79–99 Size and species diversity of zooplankton communities in Post AF, Dedej Z, Gottlieb R, Li H, Thomas D, El-Absawi M, El- fluctuating Mediterranean salt marshes. Estuar Coast Shelf Sci Naggar A, El-Gharabawi M, Sommer U (2002) Spatial and 67:424–432 temporal distribution of Trichodesmium spp. in the stratified Gulf Dahan M, Benayahu Y (1997a) Reproduction of Dendronephthya of Aqaba, Red Sea. Mar Ecol Prog Ser 239:241–250 hemprichi (Cnidaria: Octocorallia): year-round spawning in an Reiss Z, Hottinger L (1984) The Gulf of Aqaba: ecological azooxanthellate soft coral. Mar Biol 129:573–579 micropaleontology. Springer, New York 72 Mar Biodiv (2012) 42:65–72

Roney HC, Booth GM, Cox PA (2009) Competitive exclusion of Verseveldt J (1965) Report on the Octocoralia (Stolonifera and Cyanobacterial species in the Great Salt Lake. Extremophiles Alcyonacea) of the Israel South Red Sea Expedition 1962, with 13:355–361 notes on other collections from the Red Sea. Sea Fish Res Stn Rubenstein DI, Koehl MAR (1977) The mechanisms of filter feeding: Haifa Bull 14:27–47 some theoretical considerations. Am Nat 111:981–994 Verseveldt J (1970) Report on some Octocorallia (Alcyonacea) from Rutman J, Fishelson L (1969) Food composition and feeding behavior the northern Red Sea. Isr J Zool 19:209–229 of shallow-water crinoids at Eilat (Red Sea). Mar Biol 3:46–57 Vogel S (1981) Life in moving fluids, the physical biology of low. Sebens KP, Johnson AS (1991) Effect of water movement on prey Princeton University Press, New Jersey capture and distribution of reef coral. Hydrobiologia 216 Wang ZL, Zhang DY, Wang G (2005) Does spatial structure facilitate (217):247–248 coexistence of identical competitors? Ecol Model 181:17–23 Sponaugle S, LaBarbera M (1991) Drag-induced deformation - a Witman JD, Dayton PK (2001) Rocky subtidal communities. In: MD functional feeding strategy in 2 species of gorgonians. J Exp Mar Bartness, SD Gaines, ME Hay (eds) Marine community ecology. Biol Ecol 148:121–134 Sinauer, Sunderland, MA, pp 339–366 Vasconcelos P, Gaspar MB, Castro M (2006) Development of indices Yacobovitch T, Weis VM, Benayahu Y (2003) Development and for nonsacrificial sexing of imposex-affected Hexaplex (Truncu- survivorship of zooxanthellate and azooxanthellate primary lariopsis) Trunculus (Gastropoda: Muricidae). J Molluscan Stud polyps of the soft coral Heteroxenia fuscescens: laboratory and 72:285–294 field comparisons. Mar Biol 142:1055–1063